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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 4076348, 13 pages
https://doi.org/10.1155/2017/4076348
Review Article

Involvement of Mitochondrial Disorders in Septic Cardiomyopathy

1Intensive Care Department, Université de Lille, Inserm, CHU Lille, U995, Lille Inflammation Research International Center (LIRIC), Lille, France
2Département de Physiologie, CHU Martinique, Faculté de Médecine, Université des Antilles, 97200 Fort de France, France
3Université de Lille, Inserm, U995, Lille Inflammation Research International Center (LIRIC), Lille, France

Correspondence should be addressed to Sebastien Preau; moc.liamg@uaerp.bes

Received 19 May 2017; Revised 11 September 2017; Accepted 28 September 2017; Published 22 October 2017

Academic Editor: Gregory Giamouzis

Copyright © 2017 Arthur Durand et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Singer, C. S. Deutschman, C. W. Seymour et al., “The third international consensus definitions for sepsis and septic shock (sepsis-3),” JAMA, vol. 315, no. 8, pp. 801–810, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Rhodes, L. E. Evans, W. Alhazzani et al., “Surviving sepsis campaign: international guidelines for management of sepsis and septic shock: 2016,” Intensive Care Medicine, vol. 43, no. 3, pp. 304–377, 2017. View at Publisher · View at Google Scholar
  3. A. Suarez De La Rica, F. Gilsanz, and E. Maseda, “Epidemiologic trends of sepsis in western countries,” Annals of Translational Medicine, vol. 4, no. 17, p. 325, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Fleischmann, A. Scherag, N. K. J. Adhikari et al., “Assessment of global incidence and mortality of hospital-treated sepsis. current estimates and limitations,” American Journal of Respiratory and Critical Care Medicine, vol. 193, no. 3, pp. 259–272, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Vieillard-Baron, “Septic cardiomyopathy,” Annals of Intensive Care, vol. 1, no. 1, p. 6, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Charpentier, C.-E. Luyt, Y. Fulla et al., “Brain natriuretic peptide: a marker of myocardial dysfunction and prognosis during severe sepsis,” Critical Care Medicine, vol. 32, no. 3, pp. 660–665, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. W. Merx and C. Weber, “Sepsis and the heart,” Circulation, vol. 116, no. 7, pp. 793–802, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Rudiger and M. Singer, “The heart in sepsis: from basic mechanisms to clinical management,” Current Vascular Pharmacology, vol. 11, no. 2, pp. 187–195, 2013. View at Publisher · View at Google Scholar
  9. Y. Kakihana, T. Ito, M. Nakahara, K. Yamaguchi, and T. Yasuda, “Sepsis-induced myocardial dysfunction: pathophysiology and management,” Journal of Intensive Care, vol. 4, p. 22, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. I. De Kock, C. Van Daele, and J. Poelaert, “Sepsis and septic shock: pathophysiological and cardiovascular background as basis for therapy,” Acta Clinica Belgica, vol. 65, no. 5, pp. 323–329, 2010. View at Publisher · View at Google Scholar
  11. R. S. Hotchkiss, P. E. Swanson, B. D. Freeman et al., “Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction,” Critical Care Medicine, vol. 27, no. 7, pp. 1230–1251, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Barth, G. Stämmler, B. Speiser, and J. Schaper, “Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man,” Journal of Molecular and Cellular Cardiology, vol. 24, no. 7, pp. 669–681, 1992. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Brealey, M. Brand, I. Hargreaves et al., “Association between mitochondrial dysfunction and severity and outcome of septic shock,” Lancet, vol. 360, no. 9328, pp. 219–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Solomon, R. Correa, H. R. Alexander et al., “Myocardial energy metabolism and morphology in a canine model of sepsis,” American Journal of Physiology - Heart and Circulatory Physiology, vol. 266, no. 2, pp. H757–H768, 1994. View at Google Scholar
  15. V. Vanasco, T. Saez, N. D. Magnani et al., “Cardiac mitochondrial biogenesis in endotoxemia is not accompanied by mitochondrial function recovery,” Free Radical Biology & Medicine, vol. 77, pp. 1–9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Fredriksson, F. Hammarqvist, K. Strigård et al., “Derangements in mitochondrial metabolism in intercostal and leg muscle of critically ill patients with sepsis-induced multiple organ failure,” American Journal of Physiology Endocrinology and Metabolism, vol. 291, no. 5, pp. E1044–E1050, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. O. Takasu, J. P. Gaut, E. Watanabe et al., “Mechanisms of cardiac and renal dysfunction in patients dying of sepsis,” American Journal of Respiratory and Critical Care Medicine, vol. 187, no. 5, pp. 509–517, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Vakifahmetoglu-Norberg, A. T. Ouchida, and E. Norberg, “The role of mitochondria in metabolism and cell death,” Biochemical and Biophysical Research Communications, vol. 482, no. 3, pp. 426–431, 2017. View at Publisher · View at Google Scholar
  19. Y.-R. Chen and J. L. Zweier, “Cardiac mitochondria and reactive oxygen species generation,” Circulation Research, vol. 114, no. 3, pp. 524–537, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Y. Yoshinaga, M. Y. Kellermann, D. L. Valentine, and R. C. Valentine, “Phospholipids and glycolipids mediate proton containment and circulation along the surface of energy-transducing membranes,” Progress in Lipid Research, vol. 64, pp. 1–15, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. G. W. Dorn and C. Maack, “SR and mitochondria: calcium cross-talk between kissing cousins,” Journal of Molecular and Cellular Cardiology, vol. 55, pp. 42–49, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. I. Lee and M. Hüttemann, “Energy crisis: the role of oxidative phosphorylation in acute inflammation and sepsis,” Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, vol. 1842, no. 9, pp. 1579–1586, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Adrie, M. Bachelet, M. Vayssier-Taussat et al., “Mitochondrial membrane potential and apoptosis peripheral blood monocytes in severe human sepsis,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 3, pp. 389–395, 2001. View at Publisher · View at Google Scholar
  24. K. Gründler, M. Angstwurm, R. Hilge et al., “Platelet mitochondrial membrane depolarization reflects disease severity in patients with sepsis and correlates with clinical outcome,” Critical Care, vol. 18, no. 1, p. R31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Lorente, M. M. Martín, E. López-Gallardo et al., “Platelet cytochrome c oxidase activity and quantity in septic patients,” Critical Care Medicine, vol. 39, no. 6, pp. 1289–1294, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. A. M. Japiassú, A. P. S. A. Santiago, J. d. C. P. dʼAvila et al., “Bioenergetic failure of human peripheral blood monocytes in patients with septic shock is mediated by reduced F1Fo adenosine-5-triphosphate synthase activity,” Critical Care Medicine, vol. 39, no. 5, pp. 1056–1063, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Larche, S. Lancel, S. M. Hassoun et al., “Inhibition of mitochondrial permeability transition prevents sepsis-induced myocardial dysfunction and mortality,” Journal of the American College of Cardiology, vol. 48, no. 2, pp. 377–385, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. S. M. Hassoun, X. Marechal, D. Montaigne et al., “Prevention of endotoxin-induced sarcoplasmic reticulum calcium leak improves mitochondrial and myocardial dysfunction,” Critical Care Medicine, vol. 36, no. 9, pp. 2590–2596, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Preau, F. Delguste, Y. Yu et al., “Endotoxemia engages the RhoA kinase pathway to impair cardiac function by altering cytoskeleton, mitochondrial fission, and autophagy,” Antioxidants & Redox Signaling, vol. 24, no. 10, pp. 529–542, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. M. S. Joshi, M. W. Julian, J. E. Huff, J. A. Bauer, Y. Xia, and E. D. Crouser, “Calcineurin regulates myocardial function during acute endotoxemia,” American Journal of Respiratory and Critical Care Medicine, vol. 173, no. 9, pp. 999–1007, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Lancel, S. M. Hassoun, R. Favory, B. Decoster, R. Motterlini, and R. Neviere, “Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis,” Journal of Pharmacology and Experimental Therapeutics, vol. 329, no. 2, pp. 641–648, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. H. F. Galley, “Oxidative stress and mitochondrial dysfunction in sepsis,” British Journal of Anaesthesia, vol. 107, no. 1, pp. 57–64, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. D. E. Taylor, A. J. Ghio, and C. A. Piantadosi, “Reactive oxygen species produced by liver mitochondria of rats in sepsis,” Archives of Biochemistry and Biophysics, vol. 316, no. 1, pp. 70–76, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. G. C. Brown and C. E. Cooper, “Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase,” FEBS Letters, vol. 356, no. 2-3, pp. 295–298, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Clementi, G. C. Brown, M. Feelisch, and S. Moncada, “Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 13, pp. 7631–7636, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. J. P. Bolaños, S. J. Heales, S. Peuchen, J. E. Barker, J. M. Land, and J. B. Clark, “Nitric oxide-mediated mitochondrial damage: a potential neuroprotective role for glutathione,” Free Radical Biology & Medicine, vol. 21, no. 7, pp. 995–1001, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. H. B. Suliman, K. E. Welty-Wolf, M. Carraway, L. Tatro, and C. A. Piantadosi, “Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis,” Cardiovascular Research, vol. 64, no. 2, pp. 279–288, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. Q. Zang, D. L. Maass, S. J. Tsai, and J. W. Horton, “Cardiac mitochondrial damage and inflammation responses in sepsis,” Surgical Infections, vol. 8, no. 1, pp. 41–54, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Radi, M. Rodriguez, L. Castro, and R. Telleri, “Inhibition of mitochondrial electron transport by peroxynitrite,” Archives of Biochemistry and Biophysics, vol. 308, no. 1, pp. 89–95, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Boveris, S. Alvarez, and A. Navarro, “The role of mitochondrial nitric oxide synthase in inflammation and septic shock,” Free Radical Biology & Medicine, vol. 33, no. 9, pp. 1186–1193, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Escames, L. C. López, F. Ortiz et al., “Attenuation of cardiac mitochondrial dysfunction by melatonin in septic mice,” The FEBS Journal, vol. 274, no. 8, pp. 2135–2147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Ni, D. Zheng, Q. Wang et al., “Deletion of capn4 protects the heart against endotoxemic injury by preventing ATP synthase disruption and inhibiting mitochondrial superoxide generation,” Circulation: Heart Failure, vol. 8, no. 5, pp. 988–996, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Ruiz-Ramírez, O. López-Acosta, M. A. Barrios-Maya, and M. El-Hafidi, “Cell death and heart failure in obesity: role of uncoupling proteins,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 9340654, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  44. M. J. Roshon, J. A. Kline, L. R. Thornton, and J. A. Watts, “Cardiac UCP2 expression and myocardial oxidative metabolism during acute septic shock in the rat,” Shock, vol. 19, no. 6, pp. 570–6, 2003. View at Publisher · View at Google Scholar
  45. X. Wang, D. Liu, W. Chai, Y. Long, L. Su, and R. Yang, “The role of uncoupling protein 2 during myocardial dysfunction in a canine model of endotoxin shock,” Shock, vol. 43, no. 3, pp. 292–297, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Zheng, J. Lyu, S. Liu et al., “Silencing of uncoupling protein 2 by small interfering RNA aggravates mitochondrial dysfunction in cardiomyocytes under septic conditions,” International Journal of Molecular Medicine, vol. 35, no. 6, pp. 1525–1536, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. A. P. Halestrap, G. P. McStay, and S. J. Clarke, “The permeability transition pore complex: another view,” Biochimie, vol. 84, no. 2-3, pp. 153–166, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Valsecchi, C. Konrad, and G. Manfredi, “Role of soluble adenylyl cyclase in mitochondria,” Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, vol. 1842, no. 12, Part B, pp. 2555–2560, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Valsecchi, L. S. Ramos-Espiritu, J. Buck, L. R. Levin, and G. Manfredi, “cAMP and mitochondria,” Physiology, vol. 28, no. 3, pp. 199–209, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Acin-Perez, E. Salazar, M. Kamenetsky, J. Buck, L. R. Levin, and G. Manfredi, “Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation,” Cell Metabolism, vol. 9, no. 3, pp. 265–276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Neviere, F. Delguste, A. Durand, J. Inamo, E. Boulanger, and S. Preau, “Abnormal mitochondrial cAMP/PKA signaling is involved in sepsis-induced mitochondrial and myocardial dysfunction,” International Journal of Molecular Sciences, vol. 17, no. 12, article 2075, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. L. C. P. Azevedo, “Mitochondrial dysfunction during sepsis,” Endocrine, Metabolic & Immune Disorders Drug Targets, vol. 10, no. 3, pp. 214–223, 2010. View at Publisher · View at Google Scholar
  53. W. Aoi, Y. Naito, and T. Yoshikawa, “Potential role of oxidative protein modification in energy metabolism in exercise,” Sub-Cellular Biochemistry, vol. 77, pp. 175–187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. C. A. Piantadosi, C. M. Withers, R. R. Bartz et al., “Heme oxygenase-1 couples activation of mitochondrial biogenesis to anti-inflammatory cytokine expression,” The Journal of Biological Chemistry, vol. 286, no. 18, pp. 16374–16385, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Cadenas, J. Aragonés, and M. O. Landázuri, “Mitochondrial reprogramming through cardiac oxygen sensors in ischaemic heart disease,” Cardiovascular Research, vol. 88, no. 2, pp. 219–228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Sekine and H. Ichijo, “Mitochondrial proteolysis: its emerging roles in stress responses,” Biochimica et Biophysica Acta (BBA)-General Subjects, vol. 1850, no. 2, pp. 274–280, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Kroemer, L. Galluzzi, and C. Brenner, “Mitochondrial membrane permeabilization in cell death,” Physiological Reviews, vol. 87, no. 1, pp. 99–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Kroemer, B. Dallaporta, and M. Resche-Rigon, “The mitochondrial death/life regulator in apoptosis and necrosis,” Annual Review of Physiology, vol. 60, pp. 619–642, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. D. J. Hausenloy and D. M. Yellon, “New directions for protecting the heart against ischaemia-reperfusion injury: targeting the reperfusion injury salvage kinase (RISK)-pathway,” Cardiovascular Research, vol. 61, no. 3, pp. 448–460, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Nevière, H. Fauvel, C. Chopin, P. Formstecher, and P. Marchetti, “Caspase inhibition prevents cardiac dysfunction and heart apoptosis in a rat model of sepsis,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 1, pp. 218–225, 2001. View at Publisher · View at Google Scholar
  61. S. Lancel, O. Joulin, R. Favory et al., “Ventricular myocyte caspases are directly responsible for endotoxin-induced cardiac dysfunction,” Circulation, vol. 111, no. 20, pp. 2596–2604, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. W. L. Lovett, S. L. Wangensteen, T. M. Glenn, and A. M. Lefer, “Presence of a myocardial depressant factor in patients in circulatory shock,” Surgery, vol. 70, no. 2, pp. 223–231, 1971. View at Google Scholar
  63. J. E. Parrillo, C. Burch, J. H. Shelhamer, M. M. Parker, C. Natanson, and W. Schuette, “A circulating myocardial depressant substance in humans with septic shock. Septic shock patients with a reduced ejection fraction have a circulating factor that depresses in vitro myocardial cell performance,” The Journal of Clinical Investigation, vol. 76, no. 4, pp. 1539–1553, 1985. View at Publisher · View at Google Scholar
  64. A. Kumar, A. Krieger, S. Symeoneides, A. Kumar, and J. E. Parrillo, “Myocardial dysfunction in septic shock: part II. Role of cytokines and nitric oxide,” Journal of Cardiothoracic and Vascular Anesthesia, vol. 15, no. 4, pp. 485–511, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Matzinger, “Friendly and dangerous signals: is the tissue in control?” Nature Immunology, vol. 8, no. 1, pp. 11–13, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Matzinger, “The danger model: a renewed sense of self,” Science, vol. 296, no. 5566, pp. 301–305, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Zhang, M. Mo, W. Ding et al., “High-mobility group box 1 (HMGB1) impaired cardiac excitation-contraction coupling by enhancing the sarcoplasmic reticulum (SR) Ca2+ leak through TLR4-ROS signaling in cardiomyocytes,” Journal of Molecular and Cellular Cardiology, vol. 74, pp. 260–273, 2014. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Galluzzi, O. Kepp, and G. Kroemer, “Mitochondria: master regulators of danger signalling,” Nature Reviews Molecular Cell Biology, vol. 13, no. 12, pp. 780–788, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. X. Yao, J. G. Wigginton, D. L. Maass et al., “Estrogen-provided cardiac protection following burn trauma is mediated through a reduction in mitochondria-derived DAMPs,” American Journal of Physiology Heart and Circulatory Physiology, vol. 306, no. 6, pp. H882–H894, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. C. F. Wenceslau, C. G. McCarthy, T. Szasz, S. Goulopoulou, and R. C. Webb, “Mitochondrial N-formyl peptides induce cardiovascular collapse and sepsis-like syndrome,” American Journal of Physiology Heart and Circulatory Physiology, vol. 308, no. 7, pp. H768–H777, 2015. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Timmermans, M. Kox, G. J. Scheffer, and P. Pickkers, “Plasma nuclear and mitochondrial DNA levels, and markers of inflammation, shock, and organ damage in patients with septic shock,” Shock, vol. 45, no. 6, pp. 607–612, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Yamanouchi, D. Kudo, M. Yamada, N. Miyagawa, H. Furukawa, and S. Kushimoto, “Plasma mitochondrial DNA levels in patients with trauma and severe sepsis: time course and the association with clinical status,” Journal of Critical Care, vol. 28, no. 6, pp. 1027–1031, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Nakahira, S.-Y. Kyung, A. J. Rogers et al., “Circulating mitochondrial DNA in patients in the ICU as a marker of mortality: derivation and validation,” PLoS Medicine, vol. 10, no. 12, article e1001577, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Timmermans, M. Kox, M. Vaneker et al., “Plasma levels of danger-associated molecular patterns are associated with immune suppression in trauma patients,” Intensive Care Medicine, vol. 42, no. 4, pp. 551–561, 2016. View at Publisher · View at Google Scholar · View at Scopus
  75. K. Timmermans, M. Kox, J. Gerretsen et al., “The involvement of danger-associated molecular patterns in the development of immunoparalysis in cardiac arrest patients,” Critical Care Medicine, vol. 43, no. 11, pp. 2332–2338, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Unuma, T. Aki, T. Funakoshi, K. Hashimoto, and K. Uemura, “Extrusion of mitochondrial contents from lipopolysaccharide-stimulated cells: involvement of autophagy,” Autophagy, vol. 11, no. 9, pp. 1520–1536, 2015. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Yousefi, J. A. Gold, N. Andina et al., “Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense,” Nature Medicine, vol. 14, no. 9, pp. 949–953, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Maeda and B. Fadeel, “Mitochondria released by cells undergoing TNF-α-induced necroptosis act as danger signals,” Cell Death & Disease, vol. 5, no. 7, article e1312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Mijaljica, M. Prescott, and R. J. Devenish, “Mitophagy and mitoptosis in disease processes,” Methods in Molecular Biology, vol. 648, pp. 93–106, 2010. View at Publisher · View at Google Scholar
  80. R. K. Boyapati, A. Tamborska, D. A. Dorward, and G. T. Ho, “Advances in the understanding of mitochondrial DNA as a pathogenic factor in inflammatory diseases,” F1000Research, vol. 6, p. 169, 2017. View at Publisher · View at Google Scholar
  81. Q. Zhang, M. Raoof, Y. Chen et al., “Circulating mitochondrial DAMPs cause inflammatory responses to injury,” Nature, vol. 464, no. 7285, pp. 104–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. S. T. Schäfer, L. Franken, M. Adamzik et al., “Mitochondrial DNA: an endogenous trigger for immune paralysis,” Anesthesiology, vol. 124, no. 4, pp. 923–933, 2016. View at Publisher · View at Google Scholar · View at Scopus
  83. L. Zhang, S. Deng, S. Zhao et al., “Intra-peritoneal administration of mitochondrial DNA provokes acute lung injury and systemic inflammation via toll-like receptor 9,” International Journal of Molecular Sciences, vol. 17, no. 9, article 1425, 2016. View at Publisher · View at Google Scholar · View at Scopus
  84. X. Gu, G. Wu, Y. Yao et al., “Intratracheal administration of mitochondrial DNA directly provokes lung inflammation through the TLR9-p38 MAPK pathway,” Free Radical Biology & Medicine, vol. 83, pp. 149–158, 2015. View at Publisher · View at Google Scholar · View at Scopus
  85. J.-Z. Zhang, Z. Liu, J. Liu, J. X. Ren, and T. S. Sun, “Mitochondrial DNA induces inflammation and increases TLR9/NF-κB expression in lung tissue,” International Journal of Molecular Medicine, vol. 33, no. 4, pp. 817–824, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. N. Tsuji, T. Tsuji, N. Ohashi, A. Kato, Y. Fujigaki, and H. Yasuda, “Role of mitochondrial DNA in septic AKI via toll-like receptor 9,” Journal of the American Society of Nephrology, vol. 27, no. 7, pp. 2009–2020, 2016. View at Publisher · View at Google Scholar
  87. T. Oka, S. Hikoso, O. Yamaguchi et al., “Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure,” Nature, vol. 485, no. 7397, pp. 251–255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. G. W. Dorn and R. N. Kitsis, “The mitochondrial dynamism-mitophagy-cell death interactome: multiple roles performed by members of a mitochondrial molecular ensemble,” Circulation Research, vol. 116, no. 1, pp. 167–182, 2015. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Zechner, L. Lai, J. F. Zechner et al., “Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity,” Cell Metabolism, vol. 12, no. 6, pp. 633–642, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. J. J. Lehman, P. M. Barger, A. Kovacs, J. E. Saffitz, D. M. Medeiros, and D. P. Kelly, “Peroxisome proliferator-activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis,” The Journal of Clinical Investigation, vol. 106, no. 7, pp. 847–856, 2000. View at Publisher · View at Google Scholar
  91. D. A. Kubli and Å. B. Gustafsson, “Mitochondria and mitophagy: the yin and yang of cell death control,” Circulation Research, vol. 111, no. 9, pp. 1208–1221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Mai, B. Muster, J. Bereiter-Hahn, and M. Jendrach, “Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence lifespan,” Autophagy, vol. 8, no. 1, pp. 47–62, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Takikita, C. Schreiner, R. Baum et al., “Fiber type conversion by PGC-1α activates lysosomal and autophagosomal biogenesis in both unaffected and Pompe skeletal muscle,” PLoS One, vol. 5, no. 12, article e15239, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. C. M. Reynolds, H. B. Suliman, J. W. Hollingsworth, K. E. Welty-Wolf, M. S. Carraway, and C. A. Piantadosi, “Nitric oxide synthase-2 induction optimizes cardiac mitochondrial biogenesis after endotoxemia,” Free Radical Biology & Medicine, vol. 46, no. 5, pp. 564–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. D. W. Haden, H. B. Suliman, M. S. Carraway et al., “Mitochondrial biogenesis restores oxidative metabolism during Staphylococcus aureus sepsis,” American Journal of Respiratory and Critical Care Medicine, vol. 176, no. 8, pp. 768–777, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. D. L. M. Hickson-Bick, C. Jones, and L. M. Buja, “Stimulation of mitochondrial biogenesis and autophagy by lipopolysaccharide in the neonatal rat cardiomyocyte protects against programmed cell death,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 2, pp. 411–418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. J. E. Carré, J.-C. Orban, L. Re et al., “Survival in critical illness is associated with early activation of mitochondrial biogenesis,” American Journal of Respiratory and Critical Care Medicine, vol. 182, no. 6, pp. 745–751, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. S. J. Matkovich, B. Al Khiami, I. R. Efimov et al., “Widespread down-regulation of cardiac mitochondrial and sarcomeric genes in patients with sepsis,” Critical Care Medicine, vol. 45, no. 3, pp. 407–414, 2017. View at Publisher · View at Google Scholar
  99. R. Favory, S. Lancel, S. Tissier, D. Mathieu, B. Decoster, and R. Nevière, “Myocardial dysfunction and potential cardiac hypoxia in rats induced by carbon monoxide inhalation,” American Journal of Respiratory and Critical Care Medicine, vol. 174, no. 3, pp. 320–325, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. T. D. Hull, R. Boddu, L. Guo et al., “Heme oxygenase-1 regulates mitochondrial quality control in the heart,” JCI Insight, vol. 1, no. 2, article e85817, 2016. View at Publisher · View at Google Scholar
  101. H. B. Suliman, J. E. Keenan, and C. A. Piantadosi, “Mitochondrial quality-control dysregulation in conditional HO-1−/− mice,” JCI Insight, vol. 2, no. 3, article e89676, 2017. View at Publisher · View at Google Scholar
  102. L. K. Russell, C. M. Mansfield, J. J. Lehman et al., “Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor γ coactivator-1α promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner,” Circulation Research, vol. 94, no. 4, pp. 525–533, 2004. View at Publisher · View at Google Scholar · View at Scopus
  103. C.-H. Hsieh, P.-Y. Pai, H.-W. Hsueh, S. S. Yuan, and Y. C. Hsieh, “Complete induction of autophagy is essential for cardioprotection in sepsis,” Annals of Surgery, vol. 253, no. 6, pp. 1190–1200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. E. H. Carchman, J. Rao, P. A. Loughran, M. R. Rosengart, and B. S. Zuckerbraun, “Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice,” Hepatology, vol. 53, no. 6, pp. 2053–2062, 2011. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Lee, S.-J. Lee, A. A. Coronata et al., “Carbon monoxide confers protection in sepsis by enhancing Beclin 1-dependent autophagy and phagocytosis,” Antioxidants & Redox Signaling, vol. 20, no. 3, pp. 432–442, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Piquereau, R. Godin, S. Deschênes et al., “Protective role of PARK2/Parkin in sepsis-induced cardiac contractile and mitochondrial dysfunction,” Autophagy, vol. 9, no. 11, pp. 1837–1851, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. J. M. Archibald, “Endosymbiosis and eukaryotic cell evolution,” Current Biology, vol. 25, no. 19, pp. R911–R921, 2015. View at Publisher · View at Google Scholar · View at Scopus
  108. R. C. Scarpulla, “Transcriptional paradigms in mammalian mitochondrial biogenesis and function,” Physiological Reviews, vol. 88, no. 2, pp. 611–638, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. D. C. Wallace, “Mitochondrial DNA sequence variation in human evolution and disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 19, pp. 8739–8746, 1994. View at Publisher · View at Google Scholar · View at Scopus
  110. A. Torroni, T. G. Schurr, M. F. Cabell et al., “Asian affinities and continental radiation of the four founding native American mtDNAs,” American Journal of Human Genetics, vol. 53, no. 3, pp. 563–590, 1993. View at Google Scholar
  111. A. Torroni, K. Huoponen, P. Francalacci et al., “Classification of European mtDNAs from an analysis of three European populations,” Genetics, vol. 144, no. 4, pp. 1835–1850, 1996. View at Google Scholar
  112. S. V. Baudouin, D. Saunders, W. Tiangyou et al., “Mitochondrial DNA and survival after sepsis: a prospective study,” Lancet, vol. 366, no. 9503, pp. 2118–2121, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. M. A. Jiménez-Sousa, E. Tamayo, M. Guzmán-Fulgencio et al., “Mitochondrial DNA haplogroups are associated with severe sepsis and mortality in patients who underwent major surgery,” The Journal of Infection, vol. 70, no. 1, pp. 20–29, 2015. View at Publisher · View at Google Scholar · View at Scopus
  114. T. Amo, N. Yadava, and R. Oh, “Experimental assessment of bioenergetic differences caused by the common European mitochondrial DNA haplogroups H and T,” Gene, vol. 411, no. 1-2, pp. 69–76, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. L. Lorente, R. Iceta, M. M. Martín et al., “Severe septic patients with mitochondrial DNA haplogroup JT show higher survival rates: a prospective, multicenter, observational study,” PLoS One, vol. 8, no. 9, article e73320, 2013. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Lorente, R. Iceta, M. M. Martín et al., “Survival and mitochondrial function in septic patients according to mitochondrial DNA haplogroup,” Critical Care, vol. 16, no. 1, article R10, 2012. View at Publisher · View at Google Scholar · View at Scopus